Global genetic diversity, introgression, and evolutionary adaptation of indicine cattle revealed by whole genome sequencing

Ningbo Chen; Xiaoting Xia; Quratulain Hanif; Fengwei Zhang; Ruihua Dang; Bizhi Huang; Yang Lyu; Xiaoyu Luo; Hucai Zhang; Huixuan Yan; Shikang Wang; Fuwen Wang; Jialei Chen; Xiwen Guan; Yangkai Liu; Shuang Li; Liangliang Jin; Pengfei Wang; Luyang Sun; Jicai Zhang; Jianyong Liu; Kaixing Qu; Yanhong Cao; Junli Sun; Yuying Liao; Zhengzhong Xiao; Ming Cai; Lan Mu; Amam Zonaed Siddiki; Muhammad Asif; Shahid Mansoor; Masroor Ellahi Babar; Tanveer Hussain; Gamamada Liyanage Lalanie Pradeepa Silva; Neena Amatya Gorkhali; Endashaw Terefe; Gurja Belay; Abdulfatai Tijjani; Tsadkan Zegeye; Mebrate Genet Gebre; Yun Ma; Yu Wang; Yongzhen Huang; Xianyong Lan; Hong Chen; Nicola Rambaldi Migliore; Giulia Colombo; Ornella Semino; Alessandro Achilli; Mikkel-Holger S Sinding; Johannes A Lenstra; Haijian Cheng; Wenfa Lu; Olivier Hanotte; Jianlin Han; Yu Jiang; Chuzhao Lei

doi:10.1038/s41467-023-43626-z

Global genetic diversity, introgression, and evolutionary adaptation of indicine cattle revealed by whole genome sequencing

Ningbo Chen, Xiaoting Xia, Quratulain Hanif, Fengwei Zhang, Ruihua Dang, Bizhi Huang, Yang Lyu, Xiaoyu Luo, Hucai Zhang, Huixuan Yan, Shikang Wang, Fuwen Wang, Jialei Chen, Xiwen Guan, Yangkai Liu, Shuang Li, Liangliang Jin, Pengfei Wang, Luyang Sun, Jicai ZhangJianyong Liu, Kaixing Qu, Yanhong Cao, Junli Sun, Yuying Liao, Zhengzhong Xiao, Ming Cai, Lan Mu, Amam Zonaed Siddiki, Muhammad Asif, Shahid Mansoor, Masroor Ellahi Babar, Tanveer Hussain, Gamamada Liyanage Lalanie Pradeepa Silva, Neena Amatya Gorkhali, Endashaw Terefe, Gurja Belay, Abdulfatai Tijjani, Tsadkan Zegeye, Mebrate Genet Gebre, Yun Ma, Yu Wang, Yongzhen Huang, Xianyong Lan, Hong Chen, Nicola Rambaldi Migliore, Giulia Colombo, Ornella Semino, Alessandro Achilli, Mikkel-Holger S Sinding, Johannes A Lenstra, Haijian Cheng, Wenfa Lu, Olivier Hanotte, Jianlin Han, Yu Jiang, Chuzhao Lei^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Indicine cattle, also referred to as zebu (Bos taurus indicus), play a central role in pastoral communities across a wide range of agro-ecosystems, from extremely hot semiarid regions to hot humid tropical regions. However, their adaptive genetic changes following their dispersal into East Asia from the Indian subcontinent have remained poorly documented. Here, we characterize their global genetic diversity using high-quality whole-genome sequencing data from 354 indicine cattle of 57 breeds/populations, including major indicine phylogeographic groups worldwide. We reveal their probable migration into East Asia was along a coastal route rather than inland routes and we detected introgression from other bovine species. Genomic regions carrying morphology-, immune-, and heat-tolerance-related genes underwent divergent selection according to Asian agro-ecologies. We identify distinct sets of loci that contain promising candidate variants for adaptation to hot semi-arid and hot humid tropical ecosystems. Our results indicate that the rapid and successful adaptation of East Asian indicine cattle to hot humid environments was promoted by localized introgression from banteng and/or gaur. Our findings provide insights into the history and environmental adaptation of indicine cattle.

Original language	English
Article number	7803
Number of pages	13
Journal	Nature Communications
Volume	14
Issue number	1
DOIs	https://doi.org/10.1038/s41467-023-43626-z
Publication status	Published - 28 Nov 2023

Bibliographical note

Publisher Copyright:
© 2023, The Author(s).

Funding

This project was supported by grants from the National Key Research and Development Program of China (2021YFD1200400, SQ2021YFF1000041, and 2022YFF1000100) (W.L., N.C., and Y.J.), the earmarked fund for China Agriculture Research System of MOF and MARA (CARS-37) (C.L. and B.H.), the Yunnan Expert Workstations (202305AF150156), the National Natural Science Foundation of China (31872317), Foreign Young Talents Program (QN2022172008L) (C.L.), fellowships of the China Postdoctoral Science Foundation (2021T140564 and 2020M683587), the National Natural Science Foundation of China (32102523), the Shaanxi Youth Science and Technology New Star (2022KJXX-77), and High-end Foreign Experts Recruitment Plan (G2022172032L) (N.C.), Shaanxi Postdoctoral Science Foundation (2023BSHEDZZ132) (X.X.), the Program of Yunling Scholar and Yunling Cattle Special Program of Yunnan Joint Laboratory of Seeds and Seeding Industry (202205AR070001) and Construction of Yunling Cattle Technology Innovation Center and Industrialization of Achievements (2019ZG007) (B.H.), the National Natural Science Foundation of China (32072720) (Y.M.), the Chinese Government’s contribution to the CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources in Beijing (2023-YWF-ZX-02) (J.H.), the International Livestock Research Institute’s Livestock Genetics Program that was supported by the CGIAR Research Program on Livestock (CRP livestock) and sponsored by the CGIAR funding contributors to the Trust Fund ( http://www.cgiar.org/about-us/our-funders/ ), partly by the Bill and Melinda Gates Foundation and UK aid from UK Foreign, Commonwealth and Development Office (Grant Agreement OPP1127286) under the auspices of the Centre for Tropical Livestock Genetics and Health (CTLGH), established jointly by the University of Edinburgh, SRUC (Scotland’s Rural College) and ILRI (O.H.). This project was also supported by the Addis Ababa University, Ethiopia, the Italian Ministry of Education for Universities and Research (MUR) for PRIN2017 20174BTC4R (A.A.), the “Fondazione Adriano Buzzati–Traverso for the Luigi Luca Cavalli-Sforza fellowship (N.R.M.), the Carlsberg Foundation (CF20-0355) (M.H.S.S.), and the National Natural Science Foundation of China International Cooperative Research and Exchange Program (31861143014) (W.L.). Finally, we thank the High-Performance Computing (HPC) Center of Northwest A&F University (NWAFU) and Hefei Advanced Computing Center for providing computing resources and Lucia Mazzocchi for her contribution to the Y chromosome computational analysis. This project was supported by grants from the National Key Research and Development Program of China (2021YFD1200400, SQ2021YFF1000041, and 2022YFF1000100) (W.L., N.C., and Y.J.), the earmarked fund for China Agriculture Research System of MOF and MARA (CARS-37) (C.L. and B.H.), the Yunnan Expert Workstations (202305AF150156), the National Natural Science Foundation of China (31872317), Foreign Young Talents Program (QN2022172008L) (C.L.), fellowships of the China Postdoctoral Science Foundation (2021T140564 and 2020M683587), the National Natural Science Foundation of China (32102523), the Shaanxi Youth Science and Technology New Star (2022KJXX-77), and High-end Foreign Experts Recruitment Plan (G2022172032L) (N.C.), Shaanxi Postdoctoral Science Foundation (2023BSHEDZZ132) (X.X.), the Program of Yunling Scholar and Yunling Cattle Special Program of Yunnan Joint Laboratory of Seeds and Seeding Industry (202205AR070001) and Construction of Yunling Cattle Technology Innovation Center and Industrialization of Achievements (2019ZG007) (B.H.), the National Natural Science Foundation of China (32072720) (Y.M.), the Chinese Government’s contribution to the CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources in Beijing (2023-YWF-ZX-02) (J.H.), the International Livestock Research Institute’s Livestock Genetics Program that was supported by the CGIAR Research Program on Livestock (CRP livestock) and sponsored by the CGIAR funding contributors to the Trust Fund (http://www.cgiar.org/about-us/our-funders/), partly by the Bill and Melinda Gates Foundation and UK aid from UK Foreign, Commonwealth and Development Office (Grant Agreement OPP1127286) under the auspices of the Centre for Tropical Livestock Genetics and Health (CTLGH), established jointly by the University of Edinburgh, SRUC (Scotland’s Rural College) and ILRI (O.H.). This project was also supported by the Addis Ababa University, Ethiopia, the Italian Ministry of Education for Universities and Research (MUR) for PRIN2017 20174BTC4R (A.A.), the “Fondazione Adriano Buzzati–Traverso for the Luigi Luca Cavalli-Sforza fellowship (N.R.M.), the Carlsberg Foundation (CF20-0355) (M.H.S.S.), and the National Natural Science Foundation of China International Cooperative Research and Exchange Program (31861143014) (W.L.). Finally, we thank the High-Performance Computing (HPC) Center of Northwest A&F University (NWAFU) and Hefei Advanced Computing Center for providing computing resources and Lucia Mazzocchi for her contribution to the Y chromosome computational analysis.

Funders	Funder number
CAAS-ILRI	2023-YWF-ZX-02
Fondazione Adriano Buzzati
Foreign Young Talents Program	QN2022172008L
Hefei Advanced Computing Center
MARA	CARS-37
National Natural Science Foundation of China International Cooperative Research and Exchange Program	31861143014
Shaanxi Youth Science and Technology New Star	2022KJXX-77
Yunnan Expert Workstations	202305AF150156
Bill and Melinda Gates Foundation
University of Edinburgh
National Natural Science Foundation of China	31872317
Carlsbergfondet	CF20-0355
China Postdoctoral Science Foundation	2020M683587, 2021T140564, 32102523
Ministero dell’Istruzione, dell’Università e della Ricerca	PRIN2017 20174BTC4R
Northwest A and F University
Addis Ababa University
Shaanxi Province Postdoctoral Science Foundation	32072720, 2019ZG007, 2023BSHEDZZ132, 202205AR070001
Earmarked Fund for China Agriculture Research System
National Key Research and Development Program of China	2021YFD1200400, 2022YFF1000100, SQ2021YFF1000041
International Livestock Research Institute
Consortium of International Agricultural Research Centers
Scotland’s Rural College
High-end Foreign Experts Recruitment Plan of China	G2022172032L
Foreign, Commonwealth and Development Office	OPP1127286

Keywords

Alleles
Animals
Biological Evolution
Cattle
Ecosystem
Genetic Variation
Polymorphism, Single Nucleotide
Whole Genome Sequencing

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1038/s41467-023-43626-zLicence: CC BY

s41467-023-43626-zFinal published version, 3.45 MBLicence: CC BY

Cite this

Chen, N., Xia, X., Hanif, Q., Zhang, F., Dang, R., Huang, B., Lyu, Y., Luo, X., Zhang, H., Yan, H., Wang, S., Wang, F., Chen, J., Guan, X., Liu, Y., Li, S., Jin, L., Wang, P., Sun, L., ... Lei, C. (2023). Global genetic diversity, introgression, and evolutionary adaptation of indicine cattle revealed by whole genome sequencing. Nature Communications, 14(1), Article 7803. https://doi.org/10.1038/s41467-023-43626-z

@article{5d9d4eabc1b64d9296fd08740e69de42,

title = "Global genetic diversity, introgression, and evolutionary adaptation of indicine cattle revealed by whole genome sequencing",

abstract = "Indicine cattle, also referred to as zebu (Bos taurus indicus), play a central role in pastoral communities across a wide range of agro-ecosystems, from extremely hot semiarid regions to hot humid tropical regions. However, their adaptive genetic changes following their dispersal into East Asia from the Indian subcontinent have remained poorly documented. Here, we characterize their global genetic diversity using high-quality whole-genome sequencing data from 354 indicine cattle of 57 breeds/populations, including major indicine phylogeographic groups worldwide. We reveal their probable migration into East Asia was along a coastal route rather than inland routes and we detected introgression from other bovine species. Genomic regions carrying morphology-, immune-, and heat-tolerance-related genes underwent divergent selection according to Asian agro-ecologies. We identify distinct sets of loci that contain promising candidate variants for adaptation to hot semi-arid and hot humid tropical ecosystems. Our results indicate that the rapid and successful adaptation of East Asian indicine cattle to hot humid environments was promoted by localized introgression from banteng and/or gaur. Our findings provide insights into the history and environmental adaptation of indicine cattle.",

keywords = "Alleles, Animals, Biological Evolution, Cattle, Ecosystem, Genetic Variation, Polymorphism, Single Nucleotide, Whole Genome Sequencing",

author = "Ningbo Chen and Xiaoting Xia and Quratulain Hanif and Fengwei Zhang and Ruihua Dang and Bizhi Huang and Yang Lyu and Xiaoyu Luo and Hucai Zhang and Huixuan Yan and Shikang Wang and Fuwen Wang and Jialei Chen and Xiwen Guan and Yangkai Liu and Shuang Li and Liangliang Jin and Pengfei Wang and Luyang Sun and Jicai Zhang and Jianyong Liu and Kaixing Qu and Yanhong Cao and Junli Sun and Yuying Liao and Zhengzhong Xiao and Ming Cai and Lan Mu and Siddiki, \{Amam Zonaed\} and Muhammad Asif and Shahid Mansoor and Babar, \{Masroor Ellahi\} and Tanveer Hussain and Silva, \{Gamamada Liyanage Lalanie Pradeepa\} and Gorkhali, \{Neena Amatya\} and Endashaw Terefe and Gurja Belay and Abdulfatai Tijjani and Tsadkan Zegeye and Gebre, \{Mebrate Genet\} and Yun Ma and Yu Wang and Yongzhen Huang and Xianyong Lan and Hong Chen and Migliore, \{Nicola Rambaldi\} and Giulia Colombo and Ornella Semino and Alessandro Achilli and Sinding, \{Mikkel-Holger S\} and Lenstra, \{Johannes A\} and Haijian Cheng and Wenfa Lu and Olivier Hanotte and Jianlin Han and Yu Jiang and Chuzhao Lei",

note = "Publisher Copyright: {\textcopyright} 2023, The Author(s).",

year = "2023",

month = nov,

day = "28",

doi = "10.1038/s41467-023-43626-z",

language = "English",

volume = "14",

journal = "Nature Communications",

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Chen, N, Xia, X, Hanif, Q, Zhang, F, Dang, R, Huang, B, Lyu, Y, Luo, X, Zhang, H, Yan, H, Wang, S, Wang, F, Chen, J, Guan, X, Liu, Y, Li, S, Jin, L, Wang, P, Sun, L, Zhang, J, Liu, J, Qu, K, Cao, Y, Sun, J, Liao, Y, Xiao, Z, Cai, M, Mu, L, Siddiki, AZ, Asif, M, Mansoor, S, Babar, ME, Hussain, T, Silva, GLLP, Gorkhali, NA, Terefe, E, Belay, G, Tijjani, A, Zegeye, T, Gebre, MG, Ma, Y, Wang, Y, Huang, Y, Lan, X, Chen, H, Migliore, NR, Colombo, G, Semino, O, Achilli, A, Sinding, M-HS, Lenstra, JA, Cheng, H, Lu, W, Hanotte, O, Han, J, Jiang, Y & Lei, C 2023, 'Global genetic diversity, introgression, and evolutionary adaptation of indicine cattle revealed by whole genome sequencing', Nature Communications, vol. 14, no. 1, 7803. https://doi.org/10.1038/s41467-023-43626-z

TY - JOUR

T1 - Global genetic diversity, introgression, and evolutionary adaptation of indicine cattle revealed by whole genome sequencing

AU - Chen, Ningbo

AU - Xia, Xiaoting

AU - Hanif, Quratulain

AU - Zhang, Fengwei

AU - Dang, Ruihua

AU - Huang, Bizhi

AU - Lyu, Yang

AU - Luo, Xiaoyu

AU - Zhang, Hucai

AU - Yan, Huixuan

AU - Wang, Shikang

AU - Wang, Fuwen

AU - Chen, Jialei

AU - Guan, Xiwen

AU - Liu, Yangkai

AU - Li, Shuang

AU - Jin, Liangliang

AU - Wang, Pengfei

AU - Sun, Luyang

AU - Zhang, Jicai

AU - Liu, Jianyong

AU - Qu, Kaixing

AU - Cao, Yanhong

AU - Sun, Junli

AU - Liao, Yuying

AU - Xiao, Zhengzhong

AU - Cai, Ming

AU - Mu, Lan

AU - Siddiki, Amam Zonaed

AU - Asif, Muhammad

AU - Mansoor, Shahid

AU - Babar, Masroor Ellahi

AU - Hussain, Tanveer

AU - Silva, Gamamada Liyanage Lalanie Pradeepa

AU - Gorkhali, Neena Amatya

AU - Terefe, Endashaw

AU - Belay, Gurja

AU - Tijjani, Abdulfatai

AU - Zegeye, Tsadkan

AU - Gebre, Mebrate Genet

AU - Ma, Yun

AU - Wang, Yu

AU - Huang, Yongzhen

AU - Lan, Xianyong

AU - Chen, Hong

AU - Migliore, Nicola Rambaldi

AU - Colombo, Giulia

AU - Semino, Ornella

AU - Achilli, Alessandro

AU - Sinding, Mikkel-Holger S

AU - Lenstra, Johannes A

AU - Cheng, Haijian

AU - Lu, Wenfa

AU - Hanotte, Olivier

AU - Han, Jianlin

AU - Jiang, Yu

AU - Lei, Chuzhao

PY - 2023/11/28

Y1 - 2023/11/28

N2 - Indicine cattle, also referred to as zebu (Bos taurus indicus), play a central role in pastoral communities across a wide range of agro-ecosystems, from extremely hot semiarid regions to hot humid tropical regions. However, their adaptive genetic changes following their dispersal into East Asia from the Indian subcontinent have remained poorly documented. Here, we characterize their global genetic diversity using high-quality whole-genome sequencing data from 354 indicine cattle of 57 breeds/populations, including major indicine phylogeographic groups worldwide. We reveal their probable migration into East Asia was along a coastal route rather than inland routes and we detected introgression from other bovine species. Genomic regions carrying morphology-, immune-, and heat-tolerance-related genes underwent divergent selection according to Asian agro-ecologies. We identify distinct sets of loci that contain promising candidate variants for adaptation to hot semi-arid and hot humid tropical ecosystems. Our results indicate that the rapid and successful adaptation of East Asian indicine cattle to hot humid environments was promoted by localized introgression from banteng and/or gaur. Our findings provide insights into the history and environmental adaptation of indicine cattle.

AB - Indicine cattle, also referred to as zebu (Bos taurus indicus), play a central role in pastoral communities across a wide range of agro-ecosystems, from extremely hot semiarid regions to hot humid tropical regions. However, their adaptive genetic changes following their dispersal into East Asia from the Indian subcontinent have remained poorly documented. Here, we characterize their global genetic diversity using high-quality whole-genome sequencing data from 354 indicine cattle of 57 breeds/populations, including major indicine phylogeographic groups worldwide. We reveal their probable migration into East Asia was along a coastal route rather than inland routes and we detected introgression from other bovine species. Genomic regions carrying morphology-, immune-, and heat-tolerance-related genes underwent divergent selection according to Asian agro-ecologies. We identify distinct sets of loci that contain promising candidate variants for adaptation to hot semi-arid and hot humid tropical ecosystems. Our results indicate that the rapid and successful adaptation of East Asian indicine cattle to hot humid environments was promoted by localized introgression from banteng and/or gaur. Our findings provide insights into the history and environmental adaptation of indicine cattle.

KW - Alleles

KW - Animals

KW - Biological Evolution

KW - Cattle

KW - Ecosystem

KW - Genetic Variation

KW - Polymorphism, Single Nucleotide

KW - Whole Genome Sequencing

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U2 - 10.1038/s41467-023-43626-z

DO - 10.1038/s41467-023-43626-z

M3 - Article

C2 - 38016956

SN - 2041-1723

VL - 14

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 7803

ER -

Global genetic diversity, introgression, and evolutionary adaptation of indicine cattle revealed by whole genome sequencing

Abstract

Bibliographical note

Funding

Keywords

UN SDGs

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